Heat stress interferes with formation of double-strand breaks and homolog synapsis

Ning, Yingjie; Liu, Qingpei; Wang, Chong; Qin, Erdai; Wu, Zhihua; Wang, Minghui; Yang, Ke; Elesawi, Ibrahim Eid; Chen, Chunli; Liu, Hong; Qin, Rui; Liu, Bing

doi:10.1093/plphys/kiab012

Cited by 31 publications

(82 citation statements)

References 65 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Aggregated and/or enlarged ZYP1 foci hinted pairing between multiple chromosomes (Fig. 5D, G and H, blue arrows) (Loidl,1989;Morgan et al, 2017;Ning et al, 2021). Localization of SYN1 did not show any obvious defect indicating that heat stress does not affect SYN1-mediated axis (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Heat-induced DSB reduction could be one of the main causes of impaired chromosome pairing in heat-stressed Arabidopsis (Fig. 6), which, additionally, may be a conserved phenomenon among eukaryotes (Pohl and Nickoloff, 2008; Ning et al, 2021). But this effect is not likely to be caused by a direct impact on the expression of DSB formation factors (i.e., SPO11-1, PRD1, 2 and 3 ) (Ning et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…6), which, additionally, may be a conserved phenomenon among eukaryotes (Pohl and Nickoloff, 2008; Ning et al, 2021). But this effect is not likely to be caused by a direct impact on the expression of DSB formation factors (i.e., SPO11-1, PRD1, 2 and 3 ) (Ning et al, 2021). Notably, the expression of phosphatidylinositol 3 kinase-like (PI3K) protein kinase Ataxia-Telangiectasia Mutated ( ATM ), which undertakes a conserved function in sensing DNA damage and evoking DSB repair events (reviewed by (Paull, 2015)), is elevated under heat stress (Ning et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…In both dicots and monocots, low temperatures affect cytokinesis by disturbing the formation of phragmoplast, which thereby induces meiotic restitution and formation of unreduced gametes (Tang et al, 2011; De Storme et al, 2012; Liu et al, 2018). Under high temperatures, by comparison, both chromosome dynamics and cytokinesis are impacted; especially, meiotic recombination exhibits complex responses to thermal conditions (Draeger and Moore, 2017; Wang et al, 2017; Mai et al, 2019; De Storme and Geelen, 2020; Lei et al, 2020; Ning et al, 2021; Schindfessel et al, 2021). In Arabidopsis, a mild increase of temperature (28°C) positively affects type-I CO rate by enhancing the activity of ZMM proteins without impacting DSB formation (Lloyd et al, 2018; Modliszewski et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…At higher temperature (32°C), however, the rate and distribution of COs are altered and/or reshaped (De Storme and Geelen, 2020). When the temperature elevates beyond fertile threshold of Arabidopsis (36-38°C), CO formation is fully suppressed due to inhibited DSB generation and impaired homolog synapsis (Ning et al, 2021). Environmental temperatures therefore may manipulate genomic diversity, and/or influence stability of plant ploidy over generations by impacting male meiosis during microsporogenesis (Bomblies et al, 2015; Lohani et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Interfered Chromosome Pairing Promotes Meiosis Instability of Autotetraploid Arabidopsis by High Temperatures

Zhao

Ren

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Alterations of environmental temperature affect multiple meiosis processes in flowering plants. Polyploid plants derived from whole genome duplication (WGD) have enhanced genetic plasticity and tolerance to environmental stress, but meanwhile face a challenge for organization and segregation of doubled chromosome sets. In this study, we investigated the impact of increased environmental temperature on male meiosis in autotetraploid Arabidopsis thaliana. Under low to mildly-increased temperatures (5-28°C), irregular chromosome segregation universally takes place in synthesized autotetraploid Columbia-0 (Col-0). Similar meiosis lesions occur in autotetraploid rice (Oryza sativa L.) and allotetraploid canola (Brassica napus cv. Westar), but not in evolutionary-derived hexaploid wheat (Triticum aestivum). As temperature increases to extremely high, chromosome separation and tetrad formation are severely disordered due to univalent formation caused by suppressed crossing-over. We found a strong correlation between tetravalent formation and successful chromosome pairing, both of which are negatively correlated with temperature elevation, suggesting that increased temperature interferes with crossing-over prominently by impacting homolog pairing. Besides, we showed that loading irregularities of axis proteins ASY1 and ASY4 co-localize on the chromosomes of syn1 mutant, and the heat-stressed diploid and autotetraploid Col-0, revealing that heat stress affects lateral region of synaptonemal complex (SC) by impacting stability of axis. Moreover, we showed that chromosome axis and SC in autotetraploid Col-0 are more sensitive to increased temperature than that of diploid Arabidopsis. Taken together, our study provide evidence suggesting that WGD without evolutionary and/or natural adaption negatively affects stability and thermal tolerance of meiotic recombination in Arabidopsis thaliana.

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Interfered Chromosome Pairing Promotes Meiosis Instability of Autotetraploid Arabidopsis by High Temperatures

Zhao

Ren

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

The plant early recombinosome: a high security complex to break DNA during meiosis

Rafiei,

Ronceret

2024

Plant Reprod

View full text Add to dashboard Cite

Key message The formacion of numerous unpredictable DNA Double Strand Breaks (DSBs) on chromosomes iniciates meiotic recombination. In this perspective, we propose a ‘multi-key lock’ model to secure the risky but necesary breaks as well as a ‘one per pair of cromatids’ model for the topoisomerase-like early recombinosome. Abstract During meiosis, homologous chromosomes recombine at few sites of crossing-overs (COs) to ensure correct segregation. The initiation of meiotic recombination involves the formation of DNA double strand breaks (DSBs) during prophase I. Too many DSBs are dangerous for genome integrity: if these DSBs are not properly repaired, it could potentially lead to chromosomal fragmentation. Too few DSBs are also problematic: if the obligate CO cannot form between bivalents, catastrophic unequal segregation of univalents lead to the formation of sterile aneuploid spores. Research on the regulation of the formation of these necessary but risky DSBs has recently advanced in yeast, mammals and plants. DNA DSBs are created by the enzymatic activity of the early recombinosome, a topoisomerase-like complex containing SPO11. This opinion paper reviews recent insights on the regulation of the SPO11 cofactors necessary for the introduction of temporally and spatially controlled DSBs. We propose that a ‘multi-key-lock’ model for each subunit of the early recombinosome complex is required to secure the formation of DSBs. We also discuss the hypothetical implications that the established topoisomerase-like nature of the SPO11 core-complex can have in creating DSB in only one of the two replicated chromatids of early prophase I meiotic chromosomes. This hypothetical ‘one per pair of chromatids’ DSB formation model could optimize the faithful repair of the self-inflicted DSBs. Each DSB could use three potential intact homologous DNA sequences as repair template: one from the sister chromatid and the two others from the homologous chromosomes.

show abstract

Meiotic chromosome organization and its role in recombination and cancer

Morgan

Nayak

Hosoya

et al. 2023

Current Topics in Developmental Biology

View full text Add to dashboard Cite

Heat stress interferes with formation of double-strand breaks and homolog synapsis

Cited by 31 publications

References 65 publications

Interfered Chromosome Pairing Promotes Meiosis Instability of Autotetraploid Arabidopsis by High Temperatures

Interfered Chromosome Pairing Promotes Meiosis Instability of Autotetraploid Arabidopsis by High Temperatures

The plant early recombinosome: a high security complex to break DNA during meiosis

Meiotic chromosome organization and its role in recombination and cancer

Contact Info

Product

Resources

About